International Journal of Gynecology and Obstetrics 124 (2014) 248–252

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CLINICAL ARTICLE

Reproductive performance after conservative surgical treatment of postpartum hemorrhage Salah M. Rasheed a,⁎, Magdy M. Amin a, Ahmed H. Abd Ellah b, Ahmed M. Abo Elhassan c, Mazen A. El Zahry d, Hala A. Wahab e a

Department of Obstetrics and Gynecology, Sohag University, Sohag, Egypt Department of Obstetrics and Gynecology, Qena University, Qena, Egypt Department of Obstetrics and Gynecology, Assiut University, Assiut, Egypt d Department of Obstetrics and Gynecology, Al Azhar University, Cairo, Egypt e Department of Obstetrics and Gynecology, Cairo University, Cairo, Egypt b c

a r t i c l e

i n f o

Article history: Received 19 June 2013 Received in revised form 19 August 2013 Accepted 19 November 2013 Keywords: Infertility Pregnancy outcome Uterine-sparing procedures

a b s t r a c t Objective: To evaluate the impact of bilateral internal iliac artery ligation (BIL), bilateral uterine artery ligation (BUAL), step-wise uterine devascularization (SWUD), and B-Lynch on infertility, ovarian reserve, and pregnancy outcome. Methods: The study included 168 infertile or pregnant patients—recruited at outpatient clinics in Egypt— who had previously undergone uterine-sparing surgery (BIL [group I], n = 59; SWUD [group II], n = 65); BUAL [group III], n = 2; and B-Lynch [group IV], n = 42). One-way analysis of variance was used to compare the prevalence of infertility, the status of ovarian reserve, and the prevalence and type of relevant maternal and/or fetal obstetric complications between the groups. Results: Groups II and IV had the highest prevalences of infertility. The ovarian reserve was significantly lower in group II. Unexplained infertility was the predominant cause of infertility in group I, anovulation and premature ovarian failure in group II, and endometriosis and intrauterine adhesions in group IV. The frequency of obstetric complications, particularly placenta previa and preterm labor, was high in group IV. Conclusion: Of the 4 procedures, BIL had the least deleterious effect on reproductive performance; SWUD increased the risk of premature ovarian failure, and B-Lynch increased the risks of endometriosis, intrauterine adhesions, placenta previa, and preterm labor. © 2013 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction Atonic postpartum hemorrhage (PPH) is the most common form of PPH, which is in turn the dominant cause of maternal morbidity and mortality worldwide [1]. The conventional primary management of atonic PPH includes uterine fundal massage, manual exploration of the uterus, and the use of various types of oxytocics [2]. For refractory cases, however, surgical interventions have been introduced to control the bleeding. Hysterectomy is the definitive surgery for controlling blood loss, but it is a radical procedure leading to permanent loss of fertility. Alternatively, several conservative surgical procedures (so-called uterine-sparing procedures) have become available. Bilateral internal iliac artery ligation (BIL) was first described in 1960 [3]. However, the procedure still needs an experienced surgeon and fails to control the bleeding in many patients [4]. Bilateral uterine artery ligation (BUAL) has subsequently been reported to be as effective as BIL, and it has the merits of simplicity and saving time

[5]. Unfortunately, the efficacy of BUAL for controlling PPH is lower than anticipated and approximately 20% of patients subsequently need a hysterectomy [6]. In 1994, step-wise uterine devascularization (SWUD)—including bilateral ligation of the uterine and ovarian vessels—was described [7] and reported to be highly effective for controlling the bleeding. More recently, a uterine compression procedure called B-Lynch technique was advocated [8] and proved to be simple, fast, and effective for treating atonic PPH. Although these uterine-sparing procedures have the merit of preserving the uterus, data about the implications of these procedures for the patients’ future reproductive performance (fertility and pregnancy outcome) are sparse. Moreover, the influence of these interventions—in particular SWUD—on the ovarian reserve has not been studied. Therefore, the present study aimed to evaluate the influences of the different uterine-sparing procedures on future fertility, ovarian reserve, and outcome of a subsequent pregnancy. 2. Materials and methods

⁎ Corresponding author at: Department of Obstetrics and Gynecology, Faculty of Medicine, Sohag University, University Street 1, 2334, Sohag, Egypt. Tel.: + 20 932320071; fax: +20 394602963. E-mail address: [email protected] (S.M. Rasheed).

The present cross-sectional multicentric study was conducted between September 1, 2008, and September 1, 2012, at the Departments of Obstetrics and Gynecology of the university hospitals in Sohag,

0020-7292/$ – see front matter © 2013 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijgo.2013.08.018

S.M. Rasheed et al. / International Journal of Gynecology and Obstetrics 124 (2014) 248–252

Qena, Assiut, Al-Azhar, and Cairo, Egypt. During the study period, all patients (n = 293), whether infertile or pregnant, who had a history of a uterine-sparing operation for controlling intractable atonic PPH during the last delivery and who attended the outpatient clinic of a participating hospital were invited to participate in the study. The uterine-sparing procedures were carried out at any of the study hospitals, and the details of the previous surgery were obtained from the hospital records. The exclusion criteria were age of more than 35 years at the time of enrollment, obesity (body mass index [BMI, calculated as weight in kilograms divided by the square of height in meters] of more than 30), refusal to participate in the study, lost or incomplete operative documents, history of multiple uterine-sparing procedures, infertility with abnormal husband semen analysis, polycystic ovarian disease, thyroid dysfunction, hyperprolactinemia, history of pelvic inflammatory disease or pelvic surgery after the last delivery, and current pregnancy with unreliable menstrual dating, pre-existing medical illness, multiple pregnancy, previous abortion, or preterm delivery. Written consent was obtained from all participants and local institutional ethics committees provided approval. The protocol for managing infertile patients included thorough history-taking followed by complete general and gynecologic examinations. Semen analysis was then performed and evaluated according to criteria from WHO [9]. All infertile participants underwent transvaginal sonography to detect any potential uterine or adnexal pathology, measure the ovarian volume, and count the number of antral follicles. A hormonal profile (basal follicle-stimulating hormone [FSH], basal luteinizing hormone [LH], basal anti-Müllerian hormone, midluteal serum progesterone, prolactin, and thyroid hormones [T3, T4]) was obtained for all participants. The FSH, anti-Müllerian hormone, antral follicle count, and ovarian volume values were used for assessment of the participants’ ovarian reserve. As the next step, ovulation was assessed by transvaginal folliculometry and measurement of the midluteal serum progesterone level (a level of more than 31.8 nmol/L indicated normal ovulation). Absence of sonographic evidence of ovulation in association with a serum progesterone level of less than 3 ng/dL was indicative of anovulation. Progesterone levels of 9.5–31.8 nmol/L in the presence of sonographic evidence of ovulation and/or visualization of the corpus luteum were signs of a luteal-phase defect. Ovulatory patients were followed-up for at least 3 cycles, whereas anovulatory patients were treated with clomiphene citrate or gonadotropins. Hysterosalpingography followed by combined laparoscopy and hysteroscopy—if indicated—was then carried out for patients who did not conceive. Patients with a normal semen analysis, regular ovulation, a normal hormonal profile, and normal hysterosalpingography, laparoscopy, and hysteroscopy results were considered to have unexplained infertility. The recruited pregnant patients and infertile patients who conceived during the follow-up period were booked according to WHO protocol [10]. The study participants, whether pregnant or infertile, were allocated into 4 groups according to the type of uterine-sparing procedure they had previously undergone: group I, BIL (n = 59); group II, SWUD (n = 65); group III, BUAL (n = 2); and group IV, B-Lynch (n = 42). The prevalence of infertility was determined, and for infertile patients the cause of infertility and the ovarian reserve were evaluated. Pregnant patients were assessed for the prevalence and type of obstetric complications, including abortion, preterm labor, abnormal placentation, intrauterine growth restriction, and PPH. Statistical analysis was performed with SPSS version 11.5 (IBM, Armonk, NY, USA). Variables between the 4 groups were compared using 1-way analysis of variance (ANOVA) followed by post-hoc analysis of the results. P b 0.05 was considered statistically significant. The statistical analysis was performed on the per-protocol population. The required sample size for the study was difficult to calculate because of a lack of studies comparing the reproductive implications of different uterine-sparing procedures.

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3. Results During the 4-year study period, 293 patients (group I, n = 112; group II, n = 118; group III, n = 2; group IV, n = 61) were recruited (Fig. 1). The operative reports confirmed that all patients with SWUD underwent bilateral uterine and ovarian arteries ligation (step-5 SWUD). A total of 76 patients (group I, n = 30; group II, n = 34; group IV, n = 12) were excluded, whereas the remaining 217 patients were enrolled into the study. Only 2 patients underwent BUAL (group III); these patients were excluded from the study because of the small sample size. In addition, 49 patients (group I, n = 23; group II, n = 19; group IV, n = 7) dropped out during the follow-up period. The remaining 166 patients (group I, n = 59; group II, n = 65; group IV, n = 42) constituted the final study population. During the study period, 13 of the initial infertile participants (group I, n = 6; group II, n = 4; group IV, n = 3) conceived and were included in the analysis of pregnant patients (Fig. 1). The prevalence of infertility was significantly higher in groups II and IV (43.1% [n = 28] and 35.7% [n = 15], respectively) than in group I (23.7% [n = 14]; P b 0.01) (Fig. 1). Among infertile patients, age, parity, duration of infertility, BMI, basal FSH, and ovarian volume were comparable between the 3 study groups. The basal anti-Müllerian hormone level and the antral follicle count were significantly lower in group II than in groups I and IV (Table 1). In total, 48 infertile patients (11 in group I; 24 in group II; 13 in group IV) underwent combined laparoscopy and hysteroscopy. The causes of infertility were markedly different among the 3 groups. Unexplained infertility was the predominant cause in group I, anovulation and unexplained infertility in group II, and endometriosis and intrauterine adhesions in group IV (Table 1). Premature ovarian failure (FSH more than 40 IU/L in patients below the age of 40 years) was observed in 3 (10.7%) patients in group II. Their ages were 31, 29, and 26 years, respectively, their basal FSH levels were 46, 89, and 67 IU/L, and they all presented with secondary amenorrhea. Intrauterine adhesions were detected in 3 (23.1%) patients in group IV. The adhesions were grade II [11] in all patients and occupied mainly the fundal portion of the uterine cavity; they were divided hysteroscopically (data not shown). For the pregnant women, age, parity, BMI, and mode of previous or current deliveries were comparable between the 3 groups (Table 2). Obstetric complications were more common (53.3%) in group IV than in groups I and II (19.6% and 34.1%, respectively). In group I, there was no trend for a particular complication to be more prevalent. Group II had a significantly higher rate of abortion than the other 2 groups, whereas placenta previa and preterm labor were significantly more common in group IV (Table 2). 4. Discussion The surgical steps and the effectiveness of various uterine-sparing procedures for controlling atonic PPH are well established, but evidence on the implications of these procedures for subsequent reproductive performance is limited. There is a considerable lack of studies that compare the reproductive performances of patients after different uterine-sparing procedures. Moreover, the influence of uterinesparing operations, particularly bilateral ligation of ovarian arteries, on the ovarian reserve has not been studied. The paucity of data around this issue may result from patient reluctance to conceive again for fear of PPH recurrence [12]. The present study assessed the reproductive implications of BIL, SWUD, and B-Lynch in a large study population. The prevalence of infertility was highest after SWUD followed by B-Lynch; the lowest prevalence—which was comparable to the prevalence of infertility in the general population [13]—was found among patients who had undergone BIL. A decreased ovarian reserve and a high rate (10.7%) of premature ovarian failure after SWUD were other interesting findings. Although cases with premature ovarian failure after

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S.M. Rasheed et al. / International Journal of Gynecology and Obstetrics 124 (2014) 248–252 Patients assessed for eligibility (n=293)

Excluded (n=76)

Enrolled (n=217)

Multiple procedures (n=19) Abnormal semen (n=14) Obesity (n=11) Unreliable LMP (n=11) PCOD (n=9) Seeking contraception (n=8) Previous abortion (n=4)

Dropped out (n=49) Allocated to a study group (n=168)

Group I, BIL (n=59)

Group III, BUAL (n=2)

Group II, SWUD (n=65)

Infertile (n=14) Pregnant (n=45)

Group I, B-Lynch (n=42)

Infertile (n=28) Pregnant (n=37)

Conceived during follow-up (n=6)

Infertile (n=15) Pregnant (n=27)

Conceived during follow-up (n=4)

Data analysis

Data analysis

Data analysis

Excluded because of small size

Infertile (n=28) Pregnant (n=41)

Infertile (n=14) Pregnant (n=51)

Conceived during follow-up (n=3)

Infertile (n=15) Pregnant (n=30)

Fig. 1. Flow chart of the study. Abbreviations: BIL, bilateral internal iliac artery ligation; BUAL; bilateral uterine artery ligation; LMP; last menstrual period; PCOD, polycystic ovarian disease; SWUD, step-wise uterine devascularization.

SWUD have been described previously [14,15], the observation of a decreased ovarian reserve following the procedure is a novel finding that may warrant further research. Although the present study

Table 1 Characteristics, ovarian reserve, and causes of infertility among infertile patients who had previously undergone uterine-sparing surgery for postpartum hemorrhage.a b

Parameter

Group I (n = 14)

Group II (n = 28)

Group IV (n = 15)

P value

Age, y Parity Duration of infertility, y BMIc FSH, IU/L AMH, nmol/L Ovarian volume, mL3 Antral follicle count Cause of infertilityd Anovulation LPD Tubal factor Endometriosise IUA Unexplained Ovarian failure

29.2 ± 2.5 2.6 ± 0.6 3.6 ± 0.5 27.3 ± 1.8 8.6 ± 0.7 6.5 ± 0.7 13.4 ± 1.4 10.2 ± 1.4

27.7 ± 3.1 2.3 ± 1.1 3.5 ± 1.1 27.9 ± 1.2 10.5 ± 1.6 3.4 ± 0.4 10.6 ± 1.2 7.3 ± 0.8

29.6 ± 1.6 2.1 ± 0.9 4.1 ± 0.6 28.1 ± 0.9 8.1 ± 0.8 8.1 ± 0.9 13.6 ± 2.5 11.4 ± 0.6

0.841 0.916 0.494 0.936 0.358 0.021f 0.326 0.046f

2 (14.3) 3 (21.4) 2/11 (18.2) 1/11 (9.1) 0 (0.0) 6/11 (54.5) 0 (0.0)

13 (46.4) 3 (10.7) 2/24 (8.3) 1/24 (4.3) 0 (0.0) 12/24 (50.0) 3 (10.7)

3 (20.0) 0 (0.0) 1/13 (7.7) 6/13 (46.2) 3/13 (23.1) 3/13 (23.1) 0 (0.0)

b0.001g NA b0.001h b0.001i NA b0.001j NA

Abbreviations: AMH, anti-Müllerian hormone; BMI, body mass index; FSH, folliclestimulating hormone; IUA, intrauterine adhesions; LPD, luteal-phase defect; NA, not applicable for statistical analysis because of the small sample size. a Values are given as mean ± SD or number (percentage). b One-way ANOVA followed by post-hoc analysis. c Calculated as weight in kilograms divided by the square of height in meters. d Multiple causes possible. e Diagnosed by laparoscopy and histopathologic examination of the lesions. f Groups I and IV versus group II. g Group II versus groups I and IV. h Group I versus groups II and IV. i Group IV versus groups I and II. j Groups I and II versus group IV.

provided no data about the past ovarian reserve of the participants, the significantly reduced ovarian reserve among patients who underwent SWUD indicates that the impaired ovarian reserve was

Table 2 Characteristics, obstetric complications, and mode of delivery among pregnant patients who had previously undergone uterine-sparing surgery for postpartum hemorrhage.a Parameter

Group I (n = 51)

Group II (n = 41)

Group IV (n = 30)

P valueb

Age, y Parity BMIc Mode of previous delivery Vaginal 1 CD N1 CD Obstetric complicationsd Total Abortion Preterm labor Placenta previa IUGR PPH Mode of current delivery Vaginal Elective CD Emergency CD

27.3 ± 1.5 2.3 ± 0.9 28.3 ± 1.2

28.2 ± 0.8 3.1 ± 0.3 26.9 ± 2.4

28.7 ± 2.1 2.6 ± 1.2 27.5 ± 1.7

0.942 0.746 0.763

14 (27.5) 24 (47.1) 13 (25.5)

14 (34.1) 18 (43.9) 8 (19.5)

9 (30.0) 14 (46.7) 7 (23.3)

0.796 0.681 0.706

10 (19.6) 4 (7.8) 1 (2.0) 2 (3.9) 2 (3.9) 3 (5.9)

14 (34.1) 8 (19.5) 1 (2.4) 3 (7.3) 2 (4.9) 2 (4.9)

16 (53.3) 4 (13.3) 3 (10.0) 7 (23.3) 1 (3.3) 2 (6.7)

b0.001e,f b0.001e b0.001g b0.001g 0.780 0.526

6 (11.8) 42 (82.4) 3 (5.9)

6 (14.6) 32 (78.1) 3 (7.3)

2 (6.7) 27 (90.0) 1 (3.3)

0.065 0.086 0.080

Abbreviations: BMI, body mass index; CD, cesarean delivery; IUGR, intrauterine growth restriction; PPH, postpartum hemorrhage. a Values are given as mean ± SD or number (percentage). b One-way ANOVA test followed by post-hoc analysis. c Calculated as weight in kilograms divided by the square of height in meters. d Participants may have had more than 1 complication. e Groups II and IV versus group I. f Group IV versus group II. g Group IV versus groups I and II.

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a consequence of the procedure itself, and may mainly be attributable to a diminished ovarian blood flow following the procedure. The association between a diminished ovarian blood flow and a decreased ovarian reserve has been shown previously [16]. Previous studies [14,17] have reported a favorable reproductive performance after SWUD, indicating that sparing the suspensory ligament of the ovary from ligation may spare the patient from ovarian failure. The discrepancy between these findings and the present study cannot be explained for certain. However, the present data highlight that any interference with the ovarian blood flow may jeopardize subsequent ovarian blood flow. The high rate of patients with unexplained infertility in the BIL group was another important finding. This finding is in disagreement with results from previous studies [18–20] showing that BIL does not affect fertility. However, these previous studies were case reports, case series, and retrospective studies; by contrast, the present study was a large prospective study. In addition, Wagaarachchi et al. [21] also reported a high rate of infertility after BIL. Although the uterine blood flow normalizes within 3 weeks after BIL [18], subtle changes in endometrial perfusion cannot be ruled out; these changes may affect endometrial receptivity and consequently implantation [21], and may provide a possible explanation for the high rate of unexplained infertility after BIL. This hypothesis is further supported by the finding of diminished endometrial perfusion among patients who underwent uterine arteries ligation [22]. The present study reported high rates of endometriosis and intrauterine adhesions among patients with B-Lynch. Previous reports [15,23–25] have linked B-Lynch to intrauterine adhesions, either because of regional uterine ischemia induced by the compression suture or because of the development of postoperative infection and inflammation. However, the high risk of endometriosis was a surprising finding that warrants further investigation. Collagen reactions within the myometrium have been reported following B-Lynch [23]. It is possible that similar reactions following the procedure occur in the peritoneal cavity, where they might trigger an immune response with subsequent stimulation of the abnormally implanted cells. Another theory is that the pressure induced by the compression suture may squeeze some endometrial cells toward the pelvic cavity, where they then develop into endometriotic deposits. In contrast to previous studies [18,26], which reported uneventful pregnancies after B-Lynch, B-Lynch in the present study was associated with the highest frequency of obstetric complications, particularly placenta previa and preterm labor. The aforementioned studies were, however, case reports, which cannot elicit reproducible results. This high rate of abnormal placentation may intuitively be attributed to previous repeated cesarean deliveries. However, the fact that the cesarean delivery rates were comparable between the 3 groups contradicts this explanation and indicates that the risk was associated with the B-Lynch procedure. The high rates of intrauterine adhesions or uterine devascularization induced by the compression suture may provide plausible explanations for the high rate of placenta previa. In agreement with the present study, previous studies [18–21] have reported favorable maternal and fetal outcomes for patients who underwent BIL. Patients with SWUD in the present study had a significantly increased risk of abortion, compared with those who had undergone another procedure. It remains unclear whether the high rate of abortion could be explained by the diminished uterine and ovarian perfusion among patients with SWUD. Unfortunately, there is a considerable lack of data on the effect of SWUD on ovarian and uterine perfusion, and further research in this field is strongly recommended. The most evident limitation of the present study is failure to assess endometrial and uterine perfusion among infertile and pregnant patients by Doppler ultrasound. Other shortcomings include an absence

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of information about the participants’ past ovarian reserve, the small number of patients who underwent combined laparoscopy and hysteroscopy, and the exclusion of patients who underwent BUAL because of the small sample size. Despite these limitations, the present study provides reasonable insights into the reproductive implications of the various uterine-sparing operations and paves the way for future studies to answer unresolved questions. In conclusion, BIL had the least deleterious effect on reproductive performance compared with SWUD and B-lynch. Therefore, we recommend BIL as the first choice for young patients who wish to preserve their fertility. The SWUD approach was associated with the highest risks of infertility, anovulation, premature ovarian failure, and abortion. The B-lynch procedure was associated with increased risks of endometriosis, intrauterine adhesions, and obstetric complications, particularly abnormal placentation and preterm labor.

Conflict of interest The authors have no conflicts of interest.

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Reproductive performance after conservative surgical treatment of postpartum hemorrhage.

To evaluate the impact of bilateral internal iliac artery ligation (BIL), bilateral uterine artery ligation (BUAL), step-wise uterine devascularizatio...
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